Wild Birds as Hosts of Amblyomma cajennense (Fabricius, 1787) (Acari: Ixodidae)

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315 315315 315315 Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 94(3): 315-322, May/Jun. 1999

Wild Birds as Hosts of

Amblyomma cajennense

(Fabricius, 1787) (Acari: Ixodidae)

Rosario Rojas/

+

, Miguel Ângelo Marini*, Maria Teresa Zanatta Coutinho**

Curso de Pós-graduação em Ecologia, Conservação e Manejo de Vida Silvestre *Departamento de Biologia Geral **Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais,

Av. Antônio Carlos 6627, 30161-970 Belo Horizonte, MG, Brasil

We evaluated the prevalence, mean intensity and relative density of ticks in 467 wild birds of 67 species (12 families) from forest and cerrado habitats at two protected areas of Minas Gerais, between March and September 1997. Ticks collected (n=177) were identified as larvae and nymphs of Amblyo-mma cajennense and four other species of AmblyoAmblyo-mma. We report for the first time 28 bird species as hosts of the immature stages of A. cajennense, demonstrating the lack of host specificity of the larvae and nymphs. A. cajennense had 15% prevalence on birds, with a mean infestation intensity of 0.37 ticks per host sampled, and 2.5 ticks per infested bird. Prevalence varied in relation to host species, diet and between birds from forests at two successional stages. There were no differences in relation to host forest dependence, participation in mixed flocks of birds, and nest type constructed. A. cajennense is a species of medical and veterinary importance, occurring on domestic animals but is known little of its occur-rence on wildlife.

Key words: Amblyomma cajennense - birds - wild hosts - larvae - nymphs

Amblyomma cajennense (Fabricius, 1787) is an ixodid tick which parasitizes man, domestic and wild animals and is very common in Brazil. It oc-curs in the New World from southern South America to southern North America (Hoogstraal & Aeschlimann 1982) and is a known vector of Rickettsia rickettsii which causes Rocky mountain spotted fever in humans as well as being a pos-sible vector of brucella and Trypanosoma cruzi in humans (Smith 1974). It is also a possible vector of piroplasmosis in cattle and has been demon-strated to cause hematological alterations in para-sitized cattle (Serra Freire & Cunha 1987).

The life cycle of A. cajennense has four stages: egg, hexapod larvae, octopod nymph and adult (Walker 1994). The cycle of A. cajennense during its free stages and as a parasite of domestic species has been studied primarily under controlled labo-ratory conditions by Rohr (1909), Olivieri and Serra Freire (1984a, b), Souza and Serra Freire (1992), Serra Freire and Olivieri (1992), and Lopes et al. (1998)

A. cajennense is considered an eclectic ecto-parasite, both during its immature stages and pos-sibly during its adult stages, with a wide range of hosts (Hoogstraal & Aeschlimann 1982). Adults usually parasitize equids, cattle and dogs as well as several other domestic species. This species has also been found on several wild vertebrates (Aragão 1936), including rodents (Linardi et al. 1987), eden-tates (Botelho et al. 1989) and several other spe-cies of small mammals (Coutinho 1997).

There is lack of studies on the role of wild birds on the dispersal of immature stages of A. cajennense. This study presents data on wild birds as hosts and dispersers of immature stages of A. cajennense. It evaluates the prevalence, mean in-tensity and relative density of infestation on birds from forests and cerrado habitats of Minas Gerais, correlating the infestation indexes with host tax-onomy, environmental variables and ecological characteristics of the birds.

MATERIALS AND METHODS

This study was conducted at “Áreas de Proteção Especial (APE) para fins de Preservação de Mananciais” owned by “Companhia de Saneamento de Minas Gerais” (Copasa), (43o.50’W, 19o.50’S). Two study areas were sampled (1) Mutuca APE (1,250 ha) and (2) Barreiro APE (1,406 ha), located in the munici-palities of Nova Lima and Belo Horizonte, respec-tively. Vegetation at these areas is composed of cerrado, gallery forest, and dry forest (Cetec 1996). This investigation was supported by Fapemig, PRPq and

CNPq.

+_{Corresponding author. Fax: +55-31-499.2567. E-mail:}

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316 316 316 316

316 Wild Birds as Hosts of A. cajennense Rosario Rojas et al.

At Barreiro APE, the forest is a more developed dry tropical forest at a more advanced successional stage (~ 150 yrs) than the Mutuca APE forest which has gallery and dry forest at an earlier successional stage (~ 90 yrs) (Cetec 1996).

The region has distinct seasonal weather changes with warm rainy summers between No-vember and March and cool dry winters between April and October (Cetec 1983) (Fig. 1). During 1997, the study sites had a total precipitation of 2,244 mm. The mean air temperature varied sea-sonally between 18o_{C and 24}o_{C, July being the}

coolest month with mean air temperature between 14o_{C and 22}o_{C (Sistema de Controle Climatológico}

Copasa).

Birds were captured at forest fragments of 1, 2, 32, and 150 ha at Barreiro and at a 200 ha frag-ment at Mutuca. Areas sampled included forest interior, the edge of these forests and cerrado transects in Mutuca and Barreiro. Captures were conducted between March and September 1997, with 15-17 mist nets (36 mm mesh, and 12 m long by 2,5 m high), placed close to the ground and opened between 7:00 and 16:00 three to four days a week, in a different area each week. Birds were identified with the help of field guides (Hilty & Brown 1986, Dunning 1987, Ridgely & Tudor 1989 a, b). Each bird captured was weighed, metal and color banded, measured (tail, wing, tarsus, and culmen), checked for the presence of molt, brood patch, sexed when possible, and aged through cra-nial ossification. Ticks were sampled checking mostly the head, neck, and belly, because these are the areas were ticks are most often found attached to birds. Ticks were collected from the body of birds with forceps and preserved in 70% alcohol. Birds were released after sampling. For the identifica-tion of ticks we used the Clifford and Anastos (1960) and Famadas et al. (1997).

Each bird species had its prevalence (number of individuals of a host species infected with a para-site species divided by the number of hosts exam-ined), and its mean intensity (mean number of in-dividuals of a parasite species per infected host in a sample) and relative density (mean number of individuals of a parasite species per host examined) (Margolis et al. 1982). Prevalence was compared with respect to bird taxon, diet, participation in mixed species flocks (feeding aggregations of birds), nest type constructed, and sex. Environmen-tal variables such as level of forest dependence, forest edge effects, forest size effects, and seasonal variation, were also tested for differences in tick prevalence. The prevalence of ticks on birds and the variables considered were tested with Chi-square tests using Yates correction (c_Y2) when de-grees of freedom were 1. Spearman rank

correla-tion (r_s) was used to compare prevalence and for-est size and prevalence and medium inffor-estation intensity. Statistical analyses were considered sig-nificant at 5%.

RESULTS

Tick prevalence, mean intensity and relative density were evaluated for 436 birds of 59 species (9 families) of Passeriformes and 31 bird species (3 families) of non-Passeriformes (Tables I, II). Ticks collected (n=177) were identified as larvae and nymphs of A. cajennense and also of four other unidentified species of Amblyomma. Adults were never found on birds.

A. cajennense was present on 28 bird species (Table I), and four other unidentified Amblyomma species were found on the following birds: Turdus albicollis, Pyriglena leucoptera, Tolmomyias sulphurescens, Basileuterus flaveolus, Cono-pophaga lineata and Saltator similis.

Passeriformes and non-Passeriformes showed differences in prevalence values, since no ticks were found on the 31 non-passerine birds sampled whereas the passerines had a prevalence of 16% (Table II). Prevalence values varied among bird families, being highest on Formicariidae (25%) and Pipridae (20.9%). The values of the mean infesta-tion intensity were high for all passeriform fami-lies, being highest on Pipridae (5.1), Vireonidae (5.0) and Dendrocolaptidae (2.66). The highest relative infestation intensity was detected on Pipridae (1.07), Vireonidae (0.83) and Formi-cariidae (0.53) (Table I).

Tick prevalence varied significantly (c2=64.573; gl=4; p=0.000) among bird dietary groups being highest on omnivorous (21.2%) and lowest on nectarivorous (0%) birds. Birds that par-ticipate in mixed-species flocks did not differ in tick prevalence (c_Y2=0.16; df=1; p=0.691) from those that do not participate. Also, birds nest type did not show any significant relationship (c2=0.449; df=2; p=0.975) with A. cajennense prevalence. Tick prevalence also did not vary in relation to host sex. This pattern was evident both for the species with more than 10 individuals sampled as well as for males and females of all species pooled together (c_Y2=0.38; df=1, p=0.539). Birds with different levels of forest dependence did not show different prevalence of A. cajennense (c2=2.73; df=2; p=0.200).

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TABLE I

Prevalence, mean and relative infestation intensity of Amblyomma cajennense, on forest and cerrado birds at Barreiro and Mutuca, Minas Gerais,

between March and September 1997

Family Individuals Prevalencea _{Number Relative} _Mean _Variationd _Diete _Nestf _Mixed _Forest _Forest _Forest _Cerrado

(species) examined of ticks densityb _intensityc _{species dependence}h _interior _border

flocksg

Non Passeriformes

Columbidae (1) 2 0(0) 0 0 — 0

Leptotila rufaxilla 2 0(0) 0 0 — 0 F A N 2 X X

Trochilidae (6) 28 0(0) 0 0 — 0

Phaetornis pretrei 2 0(0) 0 0 — 0 N A N 2 X

Colibri serrirostris 1 0(0) 0 0 — 0 N A N 2 X

Chlorostilbon aureoventris 1 0(0) 0 0 — 0 N A N 2 X

Thalurania furcata 18 0(0) 0 0 — 0 N A N 2 X X X

Amazilia sp. 5 0(0) 0 0 — 0 N A N 3 X X X

Amazilia lactea 1 0(0) 0 0 — 0 N A N 3 X

Family Picidae (1) 1 0(0) 0 0 — 0

Picumnus cirratus 1 0(0) 0 0 — 0 I C S 2 X

Passeriformes

—-Formicariidae (6) 56 14(25.0) 30 0.53 2.14 0-7

Thamnophilus caerulescens 17 4(23.5) 5 0.29 1.25 0-2 I A S 3 X X

Thamnophilus torquatus 1 0(0) 0 0 — 0 I A S 1 X

Dysithamnus mentalis 15 4(26.6) 11 0.73 2.75 0-7 I A S 3 X X

Herpsilochmus atricapillus 2 0(0) 0 0 — 0 I A S 3 X X

Pyriglena leucoptera 4 2(50.0) 4 1 2 0-3 I F S 3 X X

Conopophaga lineata 17 4(23.5) 10 0.59 2.5 0-5 I A N 3 X X

Family Furnariidae (5) 19 2(10.5) 2 0.10 1 0-1

Synallaxis ruficapilla 4 0(0) 0 0 — 0 I F S 3 X X

Synallaxis frontalis 1 0(0) 0 0 — 0 I F S 3 X

Syndactyla rufosuperciliata 1 0(0) 0 0 — 0 I C S 3 X

Automolus leucophthalmus 11 2(18.2) 2 0.18 1 0-1 I C S 3 X X

Lochmias nematura 2 0(0) 0 0 — 0 I C N 3 X X

Dendrocolaptidae (2) 22 3(13.6) 8 0.36 2.66 0-5 I C S 3 X X X

Sittasomus griseicapillus 17 3(17.6) 8 0.47 2.66 0-5 I C S 3 X X

Lepidocolaptes fuscus 5 0(0) 0 0 — 0

Tyrannidae (14) 88 10(11.3) 20 0.23 2.0 0-6

Elaenia mesoleuca? 1 0(0) 0 0 — 0 F A N 3 X

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Elaenia chiriquensis? 1 0(0) 0 0 — 0 F A N 1 X

Elaenia obscura 2 0(0) 0 0 — 0 F A N 3 X

Mionectes rufiventris 4 1(25.0) 1 0.25 1 0-1 F F S 3 X X

Leptopogon amaurocephalus 9 0(0) 0 0 — 0 I F S 3 X X X

Phylloscates ventralis 1 1(100) 1 1 1 1 I A S 3 X

Hemitriccus margaritaceiventer 1 0(0) 0 0 — 0 I F N 2 X

Tolmomyias sulphurenscens 6 2(33.3) 4 0.66 2 0-6 I F S 3 X X

Platyrinchus mystaceus 29 3(10.3) 6 0.21 2.0 0-2 I A S 3 X X

Myiophobus fasciatus 5 1(20.0) 1 0.20 1 0-1 I F S 1 X X

Lathrotriccus euleri 21 2(9.5) 7 0.33 3.5 0-5 I A S 3 X X X

Cnemotriccus fuscatus 1 0(0) 0 0 — 0 I A N 3 X

Myiarchus ferox 5 0(0) 0 0 — 0 I C N 2 X X

Pipridae (3) 43 (9)20.9 46 1.07 5.1 0-12

Chiroxiphia caudata 19 (8)42.1 43 2.26 5.4 0-12 F A N 3 X X X

Ilicura militaris 23 0(0) 0 0 — 0 F A N 3 X X X

Schiffornis virescens 1 1(100) 3 3 3 3 I C N 3 X

Troglodytidae (1) 4 0(0) 0 0 — 0

Troglodytes aedon 4 0(0) 0 0 — 0 I A N 1 X X

Muscicapidae (5) 35 6(17.1) 12 0.34 2 0-3

Turdus rufiventris 7 1(14.3) 1 0.14 1 0-1 O A N 1 X X

Turdus leucomelas 12 3(25.0) 7 0.58 2.33 0-3 O A N 2 X X X

Turdus amaurochalinus 2 0(0) 0 0 — 0 O A N 2 X

Turdus albicollis 9 2(22.2) 4 0.44 2 0-3 O A N 3 X X

Turdus nigriceps 5 0(0) 0 0 — 0 O A N 3 X X

Vireonidae (3) 6 1(16.6) 5 0.83 5 0-5

Cyclarhis gujanensis 1 1(100) 5 5 5 5 O A S 2 X

Vireo olivaceus 3 0(0) 0 0 — 0 O A S 3 X

Hylophilus poicilotis 2 0(0) 0 0 — 0 O A S 2 X X

Emberizidae (20) 163 25(15.3) 54 0.33 2.16 0-5

Geothlypis aequinoctialis 4 0(0) 0 0 — 0 I A N 1 X

Basileuterus flaveolus 22 5(22.7) 13 0.63 2.8 0-6 I F S 3 X X X

Basileuterus hypoleucus 29 1(3.44) 1 0.03 1 0-1 I F S 3 X X X

Coereba flaveola 7 0(0) 0 0 — 0 N F S 2 X X

Schistochlamys ruficapillus 3 1(33.3) 1 0.33 1 0-1 F A S 1 X

Neothraupis fasciata 3 0(0) 0 0 — 0 F A S 1 X

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p=0.284). The birds from the older forest (Barreiro)

had higher mean tick numbers than the birds at the

younger forest (Mutuca).

The highest prevalence values were observed

at the months with the lowest precipitation (Fig.

1). The infestation peak ocurred in May and

de-clined in March and July

. The mean infestation

intensity was highest in July

, when prevalence was

lowest, showing that infestation was intense on the

few individuals infested (Fig. 2). Nymphs were

uncommon during the months sampled with the

highest values in August and September

, whereas

the larvae were more abundant than the nymphs

and had its highest ocurrence in May (Fig. 3).

There was no significant correlation between

prevalence and mean infestation intensity neither

at the family (n=8,

r

=0,479 p=0.229) nor at the

species (n=28,

r

=0.181 p=0.354) level.

flocksg

Trichothraupis melanops 29 8(27.5) 17 0.58 2.1 0-3 O A S 3 X X X

Tangara cyanocephala 2 0(0) 0 0 — 0 F A N 2 X

Tangara cayana 6 1(16.6) 3 0.5 3 0-3 O A S 1 X X X

Dacnis cayana 2 0(0) 0 0 — 0 O A N 2 X

Zonotrichia capensis 2 0(0) 0 0 — 0 O A S 1 X

Haplospiza unicolor 8 1(12.5) 1 0.13 1 1 G A N 2 X X X

Sicalis citrina 1 0(0) 0 0 — 0 G C N 1 X

Embernagra longicauda 1 1(100) 1 1 1 1 G A N 1 X

Volatinia jacarina 8 0(0) 0 0 — 0 G A N 1 X

Sporophila caerulescens 6 0(0) 0 0 — 0 G A S 1 X X

Sporophila sp. 7 0(0) 0 0 — 0 G A S 1 X X

Arremon flavirostris 3 1(33.3) 2 0.66 2 0-2 O F N 3 X

Saltator similis 16 4(25.0) 9 0.56 2.25 0-3 O A N 2 X X X

a: number of infested individuals (percentage of infestation); b: number of ticks/number of birds examined; c: number of ticks/number of birds infested; d: range of number of

ticks; e: diet; N: nectarivore; F: frugivore; G: gramnivore; I: insectivore; O: omnivore. After Hilty and Brown (1986), and Sick (1997); f :forest dependence: 1: independent;

2: semidependent; 3: dependent. After Silva (1995); g: participation in mixed species flocks of birds. S: always, regular, or occasionally; N: never. After Ridgely and Tudor

(1989), and Sick (1997); h: nest type constructed. A: open; F: closed; C: cavity (trunk or ground). After Sick (1997).

0 10 0 20 0 30 0 40 0 50 0 60 0 70 0 JF M A M J J A S O N D M onths Rainfall (mm)

0 5 10 15 20 25

Prevalence of ticks (%)

Ra in fa ll T ic k p rev al e n c e

Fig. 1: rainfall and

Amblyomma

cajennense

prevalence on birds

at Barreiro and Mutuca, Minas Gerais during 1997.

0 1 2 3 4 5 6

M ar c h A pr il M ay June Jul y A ugus t S ept em ber M ont hs

Medium and relative intensity

0 5 10 15 20 25 Prevalence of ticks

R e la tiv e in te n s ity M edi um int ens ity P rev al enc e Fig. 2: Amblyomma cajennense

prevalence and medium and

relative intensity on birds at Barreiro and Mutuca, Minas Gerais,

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320 320 320 320

during its immature stages, as suggested by Hoogstraal and Aeschlimann (1982). The hosts of the adult phase of A . cajennense include several species of wild and domestic vertebrates (Aragão 1936).

Prevalence of Amblyomma was of 15% for all birds sampled, with 0% prevalence for non-Passeriformes and 16% for non-Passeriformes (Table I). These values are similar to the ones reported by Pruett-Jones and Pruett-Jones (1991) for other spe-cies of Ixodid in forest birds of New Guinea (15.4% for all birds; 0.6% for non-Passeriformes; and 16.4% for Passeriformes). However, the total val-ues differ from the ones reported by Marini et al. (1996) for Passeriformes from the Atlantic Forest of the State of Paraná (45.5%) and from Marini and Couto (1997) for Passeriformes and non-Passeriformes captured at several forests of Minas Gerais (24.3%). These data reveal a wide varia-tion in the prevalence of ixodid ticks on birds among different geographical regions.

Our analysis also showed that there is varia-tion in the infestavaria-tion level of Amblyomma, depend-ing on the ecology and behavior of the host. The pattern of infestation ranges from host species with high infestation levels to species which are uninfected. This is evident for Passeriformes which had high mean infestation levels and especially in TABLE II

Prevalence, relative density and mean intensity of Amblyomma cajenense, on non-passeriformes and

passeriformes birds at Barreiro and Mutuca, Minas Gerais, between March and September 1997

Individuals Prevalencea _Number _Relative _Mean _Variationd

examined of ticks densityb _intensityc

Totals non passeriformes (8) 31 0(0) 0 0 0 0

Total Passeriformes (59) 436 70(16) 177 0.40 2.5 0-12

Total (67) 467 70(15) 177 0.38 2.5 0-12

a: number of infested individuals (percentage of infestation); b: number of ticks/number of birds examined;

c: number of ticks/number of birds infested; d: range of number of ticks.

TABLE III

Tick prevalence on birds of cerrado, forest border, and forest interior at Barreiro and Mutuca, Minas Gerais, between March and September 1997

Habitat Individuals Tick prevalence Chi-Square Probability

examined (%) (c

Y2)

Cerrado 90 10

Forest 349 17 2.45 0.1173

Forest interior 146 19.8

Forest border 203 15.7 0.73 0.3943

Barreiro forest 259 21.6

Mutuca forest 90 5.5 10.86 0.001

Barreiro cerrado 44 6.8

Mutuca cerrado 46 13.04 0.36 0.5506

Fig. 3: number of larvae and nymphs of Amblyomma cajennense

on birds at Barreiro and Mutuca, Minas Gerais, between April and September 1997.

0 10 20 30 40 50 60 70 80

April May June July August September Months

Number of larvae and nymphs

Larvae Nymphs

DISCUSSION

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some families (Table I). Host species with the high-est prevalence also showed high mean infhigh-estation intensity at both the family and species level. This pattern was also reported by Pruett-Jones and Pruett-Jones (1991) and Marini et al. (1996). High infestation may represent low immunity in some individuals, a decrease in health state and body condition, and a decrease in the birds’ movement ability which may increase the encounter rate with ticks, causing a further increase in the infestation probability (Pruett-Jones & Pruett-Jones 1991). The low prevalence of A. cajennense at the sampled birds may be related to their low host specificity and to the fact that A. cajennense has at least three hosts during its cycle (Travassos & Vallejo-Freire 1944).

A. cajennense have low population densities in birds, possibly due to grooming behavior which may be considered an avian defense against ecto-parasites. An evidence of grooming is the fact that ticks are encountered mostly on body parts which birds’ beaks cannot reach easily, such as the head and the neck.

Non-Passeriformes showed zero prevalence, probably because this group was mostly repre-sented by hummingbirds (Trochilidae) which do not seem to host ticks, as was observed at this study and also by Marini et al. (1996) and Marini and Couto (1997). When exchanging hosts, ticks de-pend on the frequency of encounter with their hosts (Dobson & May 1986) and the foraging behavior of hummingbirds may reduce the possibilities of such encounters.

According to Travassos and Vallejo-Freire (1944) and Serra Freire (1982), A. cajennense is found in its adult phase from late September to late March. Larvae, however, are more frequent during May and June, and nymphs during July and Sep-tember, with some variations among localities, cli-mate, temperature and hygrometry degree. Here we observed a pattern similar to the one described by the above authors for domestic animals (Figs 2, 3). Larvae and nymphs of A. cajennense can re-main up to 100 days without feeding, re-maintaining their ability to attack hosts and to complete their life cycle (Olivieri & Serra Freire 1984a, b, Souza & Serra Freire 1992, Serra Freire & Olivieri 1992). This characteristic, associated with the need for three hosts during its evolutive cycle, and their rela-tive readiness to parasitize attacking domestic and wild animals, as well as humans, enable infected individuals to inoculate infectant material during the next phase to another animal or man (Travassos & Vallejo-Freire 1944).

When habitats are destroyed, fragmented or modified, different potential hosts make contact with each other, allowing the exchange of their

associated arthropods. If these ectoparasites are vectors, the exchange of diseases may occur. Epi-demics occur easily when diseases move within new host populations which have not been exposed in their natural habitat (Gettinger & Ernest 1995). The movement of domestic species into wild areas associated with habitat fragmentation increase this risk, which could be kept to a minimum if natural communities were kept as intact as possible, and free of domestic animals.

This makes it important to know in greater de-tail the role of wild species, such as birds, as dis-persers of this tick. An integration between ecol-ogy and veterinary medicine will allow a better understanding of population dynamics of this tick.

ACKNOWLEDGMENTS

To the students of the Bird Ecology Laboratory (UFMG) for collaboration in the field work. To Bruce Alexander for English revision. To Paulo R Oliveira for criticisms and useful suggestions. To Cristina MN Lopes and Ramiro Botelho for help in tick identification. To Cemave (Ibama) for banding permission. To “Companhia de Saneamento de Minas Gerais” (Copasa) for permis-sion to work at their properties.

REFERENCES

Aragão H 1936. Ixodidas brasileiros e de alguns paizes

limitrophes. Mem Inst Oswaldo Cruz31: 759-844.

Botelho JR, Linardi PM, da Encarnação CD 1989. Interrelações entre Acari Ixodidae e hospedeiros

edentata da Serra da Canastra, Minas Gerais, Brasil.

Mem Inst Oswaldo Cruz 84: 61-64.

Cetec 1983. Diagnóstico ambiental do estado de Minas Gerais, p. 34-42. Fundação Centro Tecnológico de Minas Gerais, Belo Horizonte.

Cetec 1996. Desenvolvimento de tecnologia para o manejo de espécies nativas e recuperação de áreas degradadas de proteção das captações da Copasa Mutuca e Barreiro. Relatório Técnico Final, Fundação Centro Tecnológico de Minas Gerais, Belo Horizonte, 55 pp.

Clifford CM, Anastos G 1960. The use of chaetotaxy in the identification of larval ticks (Acarina: Ixodidae)

J Parasitol 46: 567-578.

Coutinho MTZ 1997. Guilda de Ectoparasitos de

Pequenos Mamíferos para Comparações Espaciais

e Temporais entre Ambientes, MSc Thesis, UFMG,

Belo Horizonte, 126 pp.

Dobson AP, May RM 1986. Disease and conservation,

p. 345-365. In ME Soulé, Conservation Biology. The

Science of Scarcity and Diversity, Sunderland,

Massachussets.

Dunning JS 1987. South American Birds. A Photographic

Aid to Identification, Harrowood, Pennsylvania, 230

pp.

Famadas KM, Serra Freire NM, Lanfrendi RM 1997.

Redescription of the larva of Amblyomma cajennense

(Fabricius) (Acari: Ixodidae) using optical and scannig

electron microscopy. Acarologia 38: 101-109.

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com-322 322 322 322

munity structure and the specificity of

ectopara-site associations in central Brazil. Rev Bras Biol

55: 331-341.

Hilty SL, Brown WL 1986. A Guide to the Birds of

Co-lombia, Princeton Univ. Press, Princeton, 836 pp.

Hoogstraal H, Aeschlimann A 1982. Tick-host

specific-ity. Bull Societe Entomol Suisse 55: 5-32.

Linardi PM, Teixeira VC, Botelho JR, Riveiro LS 1987. Ectoparasitos de roedores em ambientes silvestres

do município de Juiz de Fora, Minas Gerais. Mem

Inst Oswaldo Cruz 82: 137-139.

Lopes C, Leite R, Labruna M, Oliveira P, Borges L, Rodriquez Z, Carvalho H, Freitas C, Júnior C 1998.

Host specifity of Amblyomma cajennense (Fabricius,

1787) (Acari Ixodidae) with comments on the

drop-off rhythm. Mem Inst Oswaldo Cruz 93: 347-351.

Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA 1982. The use of ecological terms in

parasitol-ogy (report of an ad hoc committee of the American

Society of Parasitologists). J Parasitol 68: 131-133.

Marini MÂ, Couto D 1997. Correlações ecológicas en-tre ectoparasitos e aves de floresta de Minas Gerais, p. 210-218. In LL Leite, CH Saito (eds),

Contribuições ao Conhecimento Ecológico do

Cerrado, Depto de Ecologia, Universidade de

Brasília, Brasília.

Marini MÂ, Reinert BL, Bornschein MR, Pinto JC, Pichorim MA 1996. Ecological correlates of ectoparasitism on Atlantic Forest birds, Brazil.

Ararajuba 4: 93-103.

Olivieri JA, Serra Freire NM 1984a. Estádio larval do

ciclo biológico de Amblyomma cajennense. Arq Univ

Fed Rur RJ 7: 139-148.

Olivieri JA, Serra Freire NM 1984b. Estádio ninfal do

ciclo biológico de Amblyomma cajennense. Arq Univ

Fed Rur RJ 7: 149-156.

Pruett-Jones S, Pruett-Jones MA 1991. Analysis and ecological correlates of tick burdens in a New Guinea

avifauna, p.154-176. In JE Loye & M Zuk (eds),

Bird-parasite Interactions: Ecology, Evolution and

Behaviour, Oxford Univ. Press, Oxford.

Ridgely RS, Tudor G 1989 a. The Birds of South America,

Vol. I, Univ. Texas Press, Austin, 616 pp.

Ridgely RS, Tudor G 1989 b. The Birds of South

America, Vol. II, Univ. Texas Press, Austin, 814 pp.

Rohr CJ 1909. Estudos sobre Ixodidae do Brasil. Rio de

Janeiro. MemInst Oswaldo Cruz1: 110-117.

Serra Freire NM 1982. Epidemiologia de Amblyomma

cajennense: ocorrência estacional e comportamento

dos estádios não parasitários em pastagens do estado

do Rio de Janeiro. Arq Univ Fed Rur RJ 5: 187-193.

Serra Freire NM, Cunha DW 1987. Amblyomma

cajennense: comportamento de ninfas e adultos como

parasitos de bovinos. Rev Bras Med Vet 9: 100-103.

Serra Freire NM, Olivieri JA 1992. Estádio adulto do

ciclo de Amblyomma cajennense. Arq Fac Vet

UFRGS 20: 224-234.

Sick H 1997. Ornitologia Brasileira, Nova Fronteira,

Rio de Janeiro, 858 pp.

Silva JMC 1995. Birds of the cerrado region, South

America. Steenstrupia 21: 69-92.

Smith MW 1974. Some aspects of the ecology and

lifecycle of Amblyomma cajennense (Fabricius,

1787) in Trinidad and their influence on tick control

measures. Ann Trop Med Parasitol 69: 121-129.

Souza AP, Serra Freire NM 1992. Variação sazonal dos

estádios adultos de Amblyomma cajennense e

Anocentor nitens, como parasitas de cavalos, no

município de Itaguaí, RJ, Brasil. Rev Brasil Parasitol

Vet 1: 31-34.

Travassos J, Vallejo-Freire A 1944. Criação artificial de

Amblyomma cajennense para o preparo da vacina

contra a febre maculosa. Mem Inst Butantan 18:

145-235.

Walker A 1994. Arthropods of Humans and Domestic